Intracranial compliance in patients with COVID-19: a multicenter observational study

Abstract

Background Patients with severe coronavirus disease-19 (COVID-19) may require the use of invasive mechanical ventilation (MV) for prolonged periods. Aggressive MV parameters have been associated with changes in intracranial pressure (ICP) in patients with acute intracranial disorders. Significant ICP elevation could compromise intracranial compliance (ICC) and cerebrovascular hemodynamics (CVH). However, the effects of these parameters in individuals without neurological disorders have not yet been evaluated.

Objective To evaluate ICC in patients on MV with COVID-19 infection compared to other diagnoses, to better characterize the effects of MV and COVID-19 upon ICC. We also compared between the ICC in patients with COVID-19 who did not require MV and healthy volunteers, to assess the isolated effect of COVID-19 upon ICC.

Methods This was an exploratory, observational study with a convenience sample. The ICC was evaluated with a noninvasive ICP monitoring device. The P2/P1 ratio was calculated by dividing the amplitude of these two points, being defined as “abnormal” when P2 > P1. The statistical analysis was performed using a mixed linear model with random effects to compare the P2/P1 ratio in all four groups on the first monitoring day.

Results A convenience sample of 78 subjects (15 MV-COVID-19, 15 MV non-COVID-19, 24 non-MV-COVID-19, and 24 healthy participants) was prospectively enrolled. There was no difference in P2/P1 ratios between MV patients with and without COVID-19, nor between non-MV patients with COVID-19 and healthy volunteers. However, the P2/P1 ratio was higher in COVID-19 patients with MV use than in those without it.

Conclusion This exploratory analysis suggests that COVID-19 does not impair ICC.

Resumo

Antecedentes Pacientes com doença grave por coronavírus-19 (COVID-19) podem necessitar do uso de ventilação mecânica (VM) invasiva por um período prolongado. Parâmetros agressivos de VM têm sido associados a alterações na pressão intracraniana (PIC) em pacientes com doenças intracranianas agudas. Elevações significativas da PIC podem comprometer a complacência intracraniana (CIC) e a hemodinâmica cerebrovascular (HVC). No entanto, os efeitos desses parâmetros em indivíduos sem doenças neurológicas ainda não foram sistematicamente avaliados.

Objetivo Avaliar a CIC em pacientes em VM com COVID-19 comparados com outros diagnósticos, para melhor caracterizar os efeitos da VM e COVID-19 sobre a CIC. Também foi feita a comparação entre a CIC em pacientes com COVID-19 sem VM e voluntários saudáveis, para avaliar o efeito isolado da COVID-19 sobre a ICC.

Métodos Trata-se de um estudo exploratório, observacional com amostra por conveniência. A CIC foi avaliada com um dispositivo não invasivo de monitoramento da PIC. A relação P2/P1 foi calculada dividindo-se a amplitude desses dois pontos, sendo definida como “anormal” quando P2 > P1. A análise estatística foi realizada usando um modelo linear misto com efeitos aleatórios para comparar a relação P2/P1 nos quatro grupos no primeiro dia de monitoramento.

Resultados Uma amostra de conveniência com 78 voluntários (15 COVID-19 em VM, 15 sem COVID-19 em VM, 24 com COVID em respiração espontânea e 24 saudáveis) foram prospectivamente incluídos. Não houve diferença nas razões P2/P1 entre pacientes em VM com e sem COVID-19, nem entre pacientes sem VM com COVID-19 ou saudáveis. No entanto, a relação P2/P1 foi maior em pacientes com COVID-19 com uso de VM do que naqueles sem.

Conclusão Os dados dessa análise exploratória sugerem que a COVID-19 não prejudica a CIC.

Keywords

COVID-19 - Intracranial Pressure - Hemodynamic Brain Response - Neurophysiological Monitoring

Palavras-chave

COVID-19 - Pressão Intracraniana - Acoplamento Neurovascular - Monitorização Neurofisiológica

• References

• 1 Mao L, Jin H, Wang M. et al. Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China. JAMA Neurol 2020; 77 (06) 683-690
• 2 Donoghue M, Hsieh F, Baronas E. et al. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 2000; 87 (05) E1-E9
• 3 Carod-Artal FJ. Neurological complications of coronavirus and COVID-19. Rev Neurol 2020; 70 (09) 311-322
• 4 Harmer D, Gilbert M, Borman R, Clark KL. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett 2002; 532 (1-2): 107-110
• 5 Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem 2000; 275 (43) 33238-33243
• 6 Xia H, Lazartigues E. Angiotensin-converting enzyme 2 in the brain: properties and future directions. J Neurochem 2008; 107 (06) 1482-1494
• 7 Ohtsuki M, Morimoto SI, Izawa H. et al. Angiotensin converting enzyme 2 gene expression increased compensatory for left ventricular remodeling in patients with end-stage heart failure. Int J Cardiol 2010; 145 (02) 333-334
• 8 Varga Z, Flammer AJ, Steiger P. et al. Endothelial cell infection and endotheliitis in COVID-19. The Lancet 2020; 395: 1417-1418
• 9 Baig AM. Deleterious Outcomes in Long-Hauler COVID-19: The Effects of SARS-CoV-2 on the CNS in Chronic COVID Syndrome. ACS Chem Neurosci 2020; 11 (24) 4017-4020
• 10 Dubé M, Le Coupanec A, Wong AHM, Rini JM, Desforges M, Talbot PJ. Axonal Transport Enables Neuron-to-Neuron Propagation of Human Coronavirus OC43. J Virol 2018; 92 (17) e00404-18
• 11 Tobin MJ, Laghi F, Jubran A. Why COVID-19 silent hypoxemia is baffling to physicians. Am J Respir Crit Care Med 2020; 202 (03) 356-360
• 12 Bohmwald K, Gálvez NMS, Ríos M, Kalergis AM. Neurologic alterations due to respiratory virus infections. Frontiers in Cellular Neuroscience 2018; 12: 386
• 13 Chen C, Zhang XR, Ju ZY, He WF. [Advances in the research of cytokine storm mechanism induced by Corona Virus Disease 2019 and the corresponding immunotherapies]. Zhonghua Shao Shang Za Zhi 2020; 36: E005
• 14 Divani AA, Andalib S, Di Napoli M. et al. Coronavirus Disease 2019 and Stroke: Clinical Manifestations and Pathophysiological Insights. J Stroke Cerebrovasc Dis 2020; 29 (08) 104941
• 15 Xu Z, Shi L, Wang Y. et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med 2020; 8 (04) 420-422
• 16 Dias C, Maia I, Cerejo A. et al. Pressures, flow, and brain oxygenation during plateau waves of intracranial pressure. Neurocrit Care 2014; 21 (01) 124-132
• 17 Guyenet PG. Regulation of breathing and autonomic outflows by chemoreceptors. Compr Physiol 2014; 4 (04) 1511-1562 . Doi: 10.1002%2Fcphy.c140004
• 18 Keir DA, Duffin J, Millar PJ, Floras JS. Simultaneous assessment of central and peripheral chemoreflex regulation of muscle sympathetic nerve activity and ventilation in healthy young men. J Physiol 2019; 597 (13) 3281-3296
• 19 Portnoy HD, Chopp M. Cerebrospinal fluid pulse wave form analysis during hypercapnia and hypoxia. Neurosurgery 1981; 9 (01) 14-27
• 20 Unnerbäck M, Ottesen JT, Reinstrup P. Increased Intracranial Pressure Attenuates the Pulsating Component of Cerebral Venous Outflow. Neurocrit Care 2019; 31 (02) 273-279
• 21 Pomschar A, Koerte I, Lee S. et al. MRI evidence for altered venous drainage and intracranial compliance in mild traumatic brain injury. PLoS One 2013; 8 (02) e55447 . Doi: 10.1371%2Fjournal.pone.0055447
• 22 Borsellino B, Schultz MJ, Gama de Abreu M, Robba C, Bilotta F. Mechanical ventilation in neurocritical care patients: a systematic literature review. Expert Rev Respir Med 2016; 10 (10) 1123-1132
• 23 Robba C, Ball L, Nogas S. et al. Effects of Positive End-Expiratory Pressure on Lung Recruitment, Respiratory Mechanics, and Intracranial Pressure in Mechanically Ventilated Brain-Injured Patients. Front Physiol 2021; 12: 711273
• 24 Stevens RD, Lazaridis C, Chalela JA. The role of mechanical ventilation in acute brain injury. Neurol Clin 2008; 26 (02) 543-563
• 25 Newell DW, Aaslid R. Transcranial Doppler: clinical and experimental uses. Cerebrovasc Brain Metab Rev 1992; 4 (02) 122-143
• 26 Aaslid R. Cerebral autoregulation and vasomotor reactivity. Front Neurol Neurosci 2006; 21: 216-228
• 27 Eide PK, Sorteberg W. Association among intracranial compliance, intracranial pulse pressure amplitude and intracranial pressure in patients with intracranial bleeds. Neurol Res 2007; 29 (08) 798-802
• 28 Chen H, Menon DK, Kavanagh BP. Impact of altered airway pressure on intracranial pressure, perfusion, and oxygenation: A narrative review. Crit Care Med 2019; 47 (02) 254-263
• 29 Brasil S, Taccone FS, Wayhs SY. et al. Cerebral hemodynamics and intracranial compliance impairment in critically ill covid-19 patients: A pilot study. Brain Sci 2021; 11 (07) 874
• 30 Cuschieri S. The CONSORT statement. Saudi J Anaesth 2019; 13 (Suppl. 01) S27-S30
• 31 Schulz KF, Altman DG, Moher D. CONSORT Group. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. BMJ 2010; 340 (7748): c332
• 32 de Moraes FM, Rocha E, Barros FCD. et al. Waveform Morphology as a Surrogate for ICP Monitoring: A Comparison Between an Invasive and a Noninvasive Method. Neurocrit Care 2022; 37 (01) 219-227
• 33 Andrade RDAP, Oshiro HE, Miyazaki CK. et al. A Nanometer Resolution Wearable Wireless Medical Device for Non Invasive Intracranial Pressure Monitoring. IEEE Sens J 2021; 21 (20) 22270-22284
• 34 Cabella B, Vilela GHF, Mascarenhas S. et al. Validation of a new noninvasive intracranial pressure monitoring method by direct comparison with an invasive technique. Acta Neurochir Suppl (Wien) 2016; 122: 93-96
• 35 Lumley T, Diehr P, Emerson S, Chen L. The importance of the normality assumption in large public health data sets. Annu Rev Public Health 2002; 23: 151-169
• 36 Mohd Razali N, Bee Wah Y. Power comparisons of Shapiro-Wilk, Kolmogorov-Smirnov, Lilliefors and Anderson-Darling tests. J Stat Model Anal 2011; 2 (01) 13-14 . Available at: https://www.researchgate.net/publication/267205556_Power_Comparisons_of_Shapiro-Wilk_Kolmogorov-Smirnov_Lilliefors_and_Anderson-Darling_Tests
• 37 Torman VB, Coster R. Riboldi J. Normalidade de variáveis: métodos de verificação e comparação de alguns testes não-paramétricos por simulação | Clinical and Biomedical Research. Revista do HCPA & Faculdade de Medicina da Universidade Federal do Rio Grande do Sul [Internet];227–34. Available at: https://seer.ufrgs.br/hcpa/article/view/29874
• 38 Hess AS, Hess JR. Understanding tests of the association of categorical variables: the Pearson chi-square test and Fisher's exact test. Transfusion 2017; 57 (04) 877-879
• 39 De la Cruz R, Marshall G, Quintana FA. Logistic regression when covariates are random effects from a non-linear mixed model. Biom J 2011; 53 (05) 735-749
• 40 Saigusa Y, Eguchi S, Komori O. Generalized quasi-linear mixed-effects model. Stat Methods Med Res 2022; 31 (07) 1280-1291
• 41 Wang Z, Brumback BA, Alrwisan AA, Winterstein AG. Model-based standardization using an outcome model with random effects. Stat Med 2019; 38 (18) 3378-3394
• 42 Brasil S, Renck AC, Taccone FS. et al. Obesity and its implications on cerebral circulation and intracranial compliance in severe COVID-19. Obes Sci Pract 2021; 7 (06) 751-759 . Doi: 10.1002%2Fosp4.534
• 43 Arnold R, Issar T, Krishnan AV, Pussell BA. Neurological complications in chronic kidney disease. JRSM Cardiovasc Dis 2016; 5: 2048004016677687
• 44 Rickli C, Cosmoski LD, Dos Santos FA. et al. Use of non-invasive intracranial pressure pulse waveform to monitor patients with End-Stage Renal Disease (ESRD). PLoS One 2021; 16 (07) e0240570
• 45 Robba C, Poole D, McNett M. et al. Mechanical ventilation in patients with acute brain injury: recommendations of the European Society of Intensive Care Medicine consensus. Intensive Care Med 2020; 46 (12) 2397-2410